RAS BiologyФизиология растений Russian Journal of Plant Physiology

  • ISSN (Print) 0015-3303
  • ISSN (Online) 3034-624X

Respiratory Response of Plants with Suppression to High Light: Some Aspects of the Functional Interaction of Chloroplasts and Mitochondria

PII
S3034624X25020011-1
DOI
10.7868/S3034624X25020011
Publication type
Article
Status
Published
Authors
Volume/ Edition
Volume 72 / Issue number 2
Pages
81-99
Abstract
The energy-dissipating systems (EDS) of a photosynthetic cell — the violaxanthin cycle (VXC) in chloroplasts and the alternative respiratory pathway (AP) in mitochondria — are involved in protecting against excess light energy. The mechanisms of functional interaction of EDS are poorly understood. The aim was to study the effect of high light on respiration and AP activity in plants with suppression of encoding the VXC enzyme — violaxanthine de-epoxidase. Four-week-old plants of line and Columbia-0 wild type line (Col-0) grown at 90 mmol/(m s) were exposed to high light, 400 mmol/(m s), for 8 hours. Under stress conditions, the line showed significantly lower values of non-photochemical quenching of chlorophyll fluorescence and the level of de-epoxidation compared to the wild-type line (Col-0), which indicated the absence of zeaxanthin-dependent protection of the photosynthetic apparatus. The plants of the mutant line reacted to high light by increasing respiration due to activation of both alternative and cytochrome pathways. At the same time, the part of AP from total respiration in the line was consistently high and amounted to about 50%, regardless of the light conditions. Activation of AP and accumulation of the alternative oxidase (AOX) protein were obviously facilitated by increased expression of most AOX genes, the level of transcripts of which was higher under control conditions (0 h), but decreased by the end of the experiment. At the same time, the amount of mRNA of the most stress-inducible AOX1a gene was the lowest among all AOX genes. It is assumed that in the line the signaling pathway supported by the transcriptional factor of MYB4, a negative regulator of phenylpropanoid synthesis, is weakened. This could be the reason for the low expression of AOX1a, which contains a large number of MYB4-binding sites in the promoter, and an increased content of anthocyanins in leaves compared to Col-0. Unlike Col-0 plants, the line was characterized by half the activity of superoxide dismutase (SOD), with a predominance of Fe-SOD localized mainly in chloroplasts. However, based on the content of superoxide anion radical and hydrogen peroxide, plants of the line showed a higher level of oxidative reactions in high-light conditions compared with the wild type line. The data obtained showed a reduced ability of plants with suppression of the genes of two key components of energy-dissipating systems ( and ) to withstand stress. The results indicate the mutual regulation of the EDS of mitochondria and chloroplasts to protect against photooxidation, the importance of AOX in the modulation of respiratory function, and the existence of fast adaptive metabolic rearrangements that provide plant viability under stressful conditions.
Keywords
Arabidopsis thaliana линия с подавлением NPQ1 альтернативная оксидаза (AOX) виолаксантиндезпоксидаза дыхание окислительный стресс повышенная освещенность содержание транскриптов генов AOX супероксиддисмутаза
Date of publication
19.03.2026
Year of publication
2026
Number of purchasers
0
Views
41

References

  1. 1. Demmig-Adams B. Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin // Biochim. Biophys. Acta — Bioenerg. 1990. V. 1020. P. 1–24. https://doi.org/10.1016/0005-2728 (90)90088-L
  2. 2. Niyogi K.K., Grossman A.R., Björkman O. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion // Plant Cell. 1998. V. 10. P. 1121–1134. https://doi.org/10.1105/tpc.10.7.1121
  3. 3. Raghavendra A.S., Padmasree K. Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation // Trends Plant Sci. 2003. V. 8. P. 546–553. https://doi.org/10.1016/j.tplants.2003.09.015
  4. 4. Noguchi K., Yoshida K. Interaction between photosynthesis and respiration in illuminated leaves // Mitochondrion. 2008. V. 8. P. 87–99. https://doi.org/10.1016/j.mito.2007.09.003
  5. 5. Гармаш Е.В. Митохондриальное дыхание фотосинтезирующей клетки // Физиология растений. 2016. Т. 63. C. 17–30. https://doi.org/10.7868/S001533031506007X @@ Garmash E.V. Mitochondrial respiration of the photosynthesisizing cell. Russ. J. Plant Physiol. 2016. V. 63. P. 13–25. https://doi.org/10.1134/S1021443715060072
  6. 6. Vanlerberghe G.C., Dahal K., Alber N.A., Chadee A. Photosynthesis, respiration and growth: a carbon and energy balancing act for alternative oxidase // Mitochondrion. 2020. V. 52. P. 197–211. https://doi.org/10.1016/j.mito.2020.04.001
  7. 7. Гармаш Е.В. Сигнальные пути регуляции экспрессии генов альтернативной оксидазы растений // Физиология растений. 2022. Т. 69. C. 3–19. https://doi.org/10.31857/S001533032010055 @@ Garmash E.V. Signal pathways for regulation of plant alternative oxidase genes’ expression. Russ. J. Plant Physiol. 2022. V. 69. P. 3–19. (In Russ.) https://doi.org/10.1134/S102144372010058
  8. 8. Van Aken O. Mitochondrial redox systems as central hubs in plant metabolism and signalling // Plant Physiol. 2021. V. 186. P. 36–52. https://doi.org/10.1093/plphys/kiab101
  9. 9. van Lis R., Atteia A. Control of mitochondrial function via photosynthetic redox signals // Photosynth. Res. 2004. V. 79. P. 133–148. https://doi.org/10.1023/B:PRES.0000015409.14871.68
  10. 10. Юрина Н.П., Одинцов М.С. Ретроградная сигнальная система хлоропластов // Физиология растений. 2019. Т. 66. C. 243–255. https://doi.org/10.1134/S0015330319040146 @@ Yurina N.P., Odintsova M.S. Chloroplast retrograde signaling system. Russ. J. Plant Physiol. 2019. V. 66. P. 509–520. https://doi.org/10.1134/S1021443719040149
  11. 11. Garmash E.V., Dymova O.V., Malyshev R.V., Plyusnina S.N., Golovko T.K. Developmental changes in energy dissipation in etiolated wheat seedlings during the greening process // Photosynthetica. 2013. V. 51. P. 497–508. https://doi.org/10.1007/s11099-013-0044-z
  12. 12. Vishwakarma A., Tetali S.D., Selinski J., Scheibe R., Padmasree K. Importance of the alternative oxidase (AOX) pathway in regulating cellular redox and ROS homeostasis to optimize photosynthesis during restriction of the cytochrome oxidase pathway in Arabidopsis thaliana // Ann Bot. 2015. V. 116. P. 555–569. https://doi.org/10.1093/aob/mcv122
  13. 13. Garmash E.V., Dymova O.V., Silina E.V., Malyshev R.V., Belykh E.S., Shelyakin M.A., Velegzhaninov I.O. AOX1a Expression in Arabidopsis thaliana affects the state of chloroplast photoprotective systems under moderately high light conditions // Plants. 2022. V. 11. P. 3030. https://doi.org/10.3390/plants11223030
  14. 14. Garmash E.V. Suppression of mitochondrial alternative oxidase can result in upregulation of the ROS scavenging network: some possible mechanisms underlying the compensation effect // Plant Biol. 2022. V. 25. P. 43–53. https://doi.org/10.1111/plb.13477
  15. 15. Boyes D.C., Zayed A.M., Ascenzi R., McCaskill A.J., Hoffman N.E., Davis K.R., Görlach J. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants // Plant Cell. 2001. V. 13. P. 1499–1510. https://doi.org/10.2307/3871382
  16. 16. Czechowski T., Stitt M., Altmann T., Udvardi M.K., Scheible W.-R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis // Plant Physiol. 2005. V. 139. P. 5–17. https://doi.org/10.1104/pp.105.063743
  17. 17. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) method // Methods. 2001. V. 25. P. 402–408. https://doi.org/10.1006/meth.2001.1262
  18. 18. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding // Anal. Biochem. 1976. V. 72. P. 248–254. https://doi.org/10.1016/0003-2697 (76)90527-3
  19. 19. Chaitanya K.S.K., Naithani S.C. Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn.f. // New Phytol. 1994. V. 126. P. 623–627. https://doi.org/10.1111/j.1469-8137.1994.tb02957.x
  20. 20. Bellincampi D., Dipierro N., Salvi G., Cervone F., De Lorenzo G. Extracellular HO induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants // Plant Physiol. 2000. V. 122. P. 1379–1386. https://doi.org/10.1104/pp.122.4.1379
  21. 21. Libik M., Konieczny R., Surowka E., Miszalski Z. Superoxide dismutase activity in organs of Mesembryanthemum crystallinum L. at different stages of CAM development // Acta Biol. Cracov. Bot. 2005. V. 47. P. 199–204.
  22. 22. Beauchamp C., Fridovich I. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels // Anal. Biochem. 1971. V. 44. P. 276–287. https://doi.org/10.1016/0003-2697 (71)90370-8
  23. 23. Giusti M.M., Wrolstad R.E. Characterization and measurement of anthocyanins by UV-visible spectroscopy // Curr. Proto. Food Anal. Chem. 2001. V. 00. P. 1.2.1–1.2.13. https://doi.org/10.1002/0471142913.faf0102s00
  24. 24. Külheim C., Jansson S. What leads to reduced fitness in non-photochemical quenching mutants? // Physiol. Plant. 2005. V. 125. P. 202–211. https://doi.org/10.1111/j.1399-3054.2005.00547.x
  25. 25. Clifton R., Millar A.H., Whelan J. Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses // Biochim. Biophys. Acta. 2006. V. 1757. P. 730–741. https://doi.org/10.1016/j.bbabio.2006.03.009
  26. 26. Yoshida K., Noguchi K. Differential gene expression profiles of the mitochondrial respiratory components in illuminated Arabidopsis leaves // Plant Cell Physiol. 2009. V. 50. P. 1449–1462. https://doi.org/10.1093/pcp/pcp090
  27. 27. Garmash E.V., Belykh E.S., Velegzhaninov I.O. The gene expression profiles of mitochondrial respiratory components in Arabidopsis plants with differing amounts of ALTERNATIVE OXIDASE1a under high intensity light // Plant Signal Behav. 2021. V. 16. https://doi.org/10.1080/15592324.2020.1864962
  28. 28. Keunen E., Schellingen K., Van Der Straeten D., Remans T., Colpaert J., Vangronsveld J., Cuypers A. ALTERNATIVE OXIDASE1a modulates the oxidative challenge during moderate Cd exposure in Arabidopsis thaliana leaves // J. Exp. Bot. 2015. V. 66. P. 2967–2977. https://doi.org/10.1093/jxb/erv035
  29. 29. Clifton R., Lister R., Parker K.L., Sappl P.G., Elhafez D., Millar A.H., Day D.A., Whelan J. Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana // Plant Mol. Biol. 2005. V. 58. P. 193–212. https://doi.org/10.1007/s11103-005-5514-7
  30. 30. Wang H., Huang J., Liang X., Bi Y. Involvement of hydrogen peroxide, calcium, and ethylene in the induction of the alternative pathway in chilling-stressed Arabidopsis callus // Planta. 2012. V. 235. P. 53–67. https://doi.org/10.1007/s00425-011-1488-7
  31. 31. Rasmusson A.G., Escobar M. Light and diurnal regulation of plant respiratory gene expression // Physiol. Plant. 2007. V. 129. P. 57–67. https://doi.org/10.1111/j.1399-3054.2006.00797.x
  32. 32. Florez-Sarasa I., Ostaszewska M., Galle A., Flexas J., Rychter A.M., Ribas-Carbó M. Changes of alternative oxidase activity, capacity and protein content in leaves of Cucumis sativus wild type and MSC16 mutant grown under different light intensities // Physiol. Plant. 2009. V. 137. P. 419–426. https://doi.org/10.1111/j.1399-3054.2009.01244.x
  33. 33. Garmash E.V., Grabelhych O.I., Velegzhaninov I.O., Borovik O.A., Dalke I.V., Voinikov V.K., Golovko T.K. Light regulation of alternative oxidase pathway during greening of etiolated wheat seedlings // J. Plant Physiol. 2015. V. 174. P. 75–84. https://doi.org/10.1016/j.jplph.2014.09.016
  34. 34. Zalutskaya Z., Lapina T., Ermilova E. The Chlamydomonas reinhardtii alternative oxidase 1 is regulated by heat stress // Plant Physiol. Biochem. 2015. V. 97. P. 229–234. https://doi.org/10.1016/j.plaphy.2015.10.014
  35. 35. El-Brolosy M.A., Stainier D.Y.R. Genetic compensation: a phenomenon in search of mechanisms // PLoS Genet 2017. V. 13. P. e1006780. https://doi.org/10.1371/journal.pgen.1006780
  36. 36. Selinski J., Hartmann A., Deckers-Hebestreit G., Day D.A., Whelan J., Scheibe R. Alternative oxidase isoforms are differentially activated by tricarboxylic acid cycle intermediates // Plant Physiol. 2018. V. 176. P. 1423–1432. https://doi.org/10.1104/pp.17.01331
  37. 37. Ambawat S., Sharma P., Yadav N.R., Yadav R.C. MYB transcription factor genes as regulators for plant responses: an overview // Physiol. Mol. Biol. Plants. 2013. V. 19. P. 307–321. https://doi.org/10.1007/s12298-013-0179-1
  38. 38. Zhang X., Ivanova A., Vandepoele K., Radomiljac J., Van de Velde J., Berkowitz O., Willems P., Xu Y., Ng S., Van Aken O., Duncan O., Zhang B., Storme V., Chan K.X., Vaneechoutte D. et al. The transcription factor MYB29 is a regulator of ALTERNATIVE OXIDASE1a // Plant Physiol. 2017. V. 173. P. 1824–1843. https://doi.org/10.1104/pp.16.01494
  39. 39. Jin H. Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis // EMBO J. 2000. V. 19. P. 6150–6161. https://doi.org/10.1093/emboj/19.22.6150
  40. 40. Shams M., Pokora W., Khadivi A., Aksmann A. Superoxide dismutase in Arabidopsis and Chlamydomonas: diversity, localization, regulation, and role // Plant Soil. 2024. V. 53. P. 751–771. https://doi.org/10.1007/s11104-024-06618-6
QR
Translate

Indexing

Scopus

Scopus

Scopus

Crossref

Scopus

Higher Attestation Commission

At the Ministry of Education and Science of the Russian Federation

Scopus

Scientific Electronic Library